Chloroplast Protein Turnover: The Influence of Extraplastidic Processes, Including Autophagy

Abstract

Most assimilated nutrients in the leaves of land plants are stored in chloroplasts as photosynthetic proteins, where they mediate CO₂ assimilation during growth. During senescence or under suboptimal conditions, chloroplast proteins are degraded, and the amino acids released during this process are used to produce young tissues, seeds, or respiratory energy. Protein degradation machineries contribute to the quality control of chloroplasts by removing damaged proteins caused by excess energy from sunlight. Whereas previous studies revealed that chloroplasts contain several types of intraplastidic proteases that likely derived from an endosymbiosed prokaryotic ancestor of chloroplasts, recent reports have demonstrated that multiple extraplastidic pathways also contribute to chloroplast protein turnover in response to specific cues. One such pathway is autophagy, an evolutionarily conserved process that leads to the vacuolar or lysosomal degradation of cytoplasmic components in eukaryotic cells. Here, we describe and contrast the extraplastidic pathways that degrade chloroplasts. This review shows that diverse pathways participate in chloroplast turnover during sugar starvation, senescence, and oxidative stress. Elucidating the mechanisms that regulate these pathways will help decipher the relationship among the diverse pathways mediating chloroplast protein turnover.

Keywords: Rubisco-containing bodies; autophagy; chlorophagy; chloroplasts; photooxidative damage; plants; senescence; sugar starvation; ubiquitin proteasome system; vacuole.

Figure 1

Schematic model for the Rubisco-containing body (RCB) pathway and chlorophagy forms of chloroplast-related autophagy. (a) When photosynthetic energy production of whole plants is impaired due to complete darkness, a portion of the chloroplast stroma is transported to the central vacuole via RCBs, which are a type of autophagic compartment that specifically contains stromal proteins. The RCB pathway can facilitate the recycling of amino acids as an energy source. (b) When senescence is accelerated in individually darkened leaves, the active production of RCBs leads to chloroplast shrinkage, thereby allowing the transport of entire chloroplasts to the vacuole via chlorophagy. (c) Photodamage from exposure to ultraviolet-B (UV-B), strong visible light, or natural sunlight causes chloroplasts to collapse. The collapsed chloroplasts are then transported to the vacuole without prior activation of RCBs. This process is suggested to serve as a quality control mechanism that removes damaged chloroplasts.

Figure 2

Schematic model for chloroplast protein turnover mediated by ATI bodies, CV-containing vesicles (CCVs), senescence-associated vacuoles (SAVs), or ubiquitination. (a) Plastid-associated ATI bodies are produced in chloroplasts and are then delivered into the central vacuole via an autophagy-dependent pathway. ATI bodies transport thylakoid, stroma, and envelope proteins. CV protein also interacts with thylakoid and stroma proteins, and then induces the production of CCVs that transport thylakoid, stroma, and envelope proteins into the central vacuole via an autophagy-independent pathway. SAVs are small lytic compartments that form in the cytoplasm. Stroma components are incorporated into the SAVs for digestion. (b) Chloroplast outer envelope-anchored E3 ligase, SP1, ubiquitinates TOC proteins and facilitates their degradation by 26S proteasome. Cytoplasmic E3 ligase PUB4 ubiquitinates oxidative chloroplasts accumulating ¹O₂ for the digestion of such chloroplasts in their entirety.